Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep
We previously demonstrated that seizure occurrences at different zeitgeber times alter sleep and circadian rhythm differently. On the other hand, the synchronized delta wave of electroencephalogram (EEG) during non-rapid eye movement (NREM) sleep facilitates seizure, while the desynchronized EEG of...
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Frontiers Media S.A.
2020-08-01
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| Series: | Frontiers in Neurology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fneur.2020.00752/full |
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| author | Hsin-Tzu Tseng Yi-Tse Hsiao Pei-Lu Yi Fang-Chia Chang Fang-Chia Chang Fang-Chia Chang Fang-Chia Chang |
| author_facet | Hsin-Tzu Tseng Yi-Tse Hsiao Pei-Lu Yi Fang-Chia Chang Fang-Chia Chang Fang-Chia Chang Fang-Chia Chang |
| author_sort | Hsin-Tzu Tseng |
| collection | DOAJ |
| description | We previously demonstrated that seizure occurrences at different zeitgeber times alter sleep and circadian rhythm differently. On the other hand, the synchronized delta wave of electroencephalogram (EEG) during non-rapid eye movement (NREM) sleep facilitates seizure, while the desynchronized EEG of rapid eye movement (REM) sleep suppresses it. We also elucidated that unilateral deep brain stimulation (DBS) of the anterior nucleus of thalamus (ANT) suppresses seizure recurrence. In the present study, we intraperitoneally injected pentylenetetrazol (PTZ, 40 mg/kg) for 14 consecutive days (PTZ kindling) to induce spontaneous seizure in rats, and a 30-min (delivered 10 min before each PTZ injection) or a 3-h DBS of unilateral ANT (delivered 1 h before each PTZ injection) was applied to suppress seizure. The frequency of DBS stimulation was 200 Hz and the electrical current consisted of biphasic square pulses with 50-μA intensity, 100-μs pulse width, and 4.1-ms stimulation interval. Our results found that PTZ-induced spontaneous seizure did not cause a significant change in the quantity of NREM sleep but suppressed the amount of REM sleep. Unilateral ANT DBS prolonged the onset latency of ictal seizure, decreased the spontaneous seizure duration, and increased the survival rate but did not change the amplitude of epileptiform EEGs during ictal period. Unilateral ANT DBS did not significantly alter NREM sleep but increased the amount of REM sleep. An analysis of the spectrograms of fast Fourier transform indicated that the intensities of all frequencies were enhanced during the PTZ-induced ictal period and the subsequent spontaneous seizure. Thirty minutes of unilateral ANT DBS suppressed the augmentation of low-frequency (<10 Hz) intensities during the spontaneous seizure induced by PTZ kindling. We further found that consecutive injections of PTZ progressively increased the enhancement of the delta powers during NREM sleep, whereas unilateral ANT DBS inhibited this progressive enhancement. It was also noticed that 30 min of ANT DBS exhibited a better efficacy in epilepsy suppression than 3 h of ANT DBS. These results elucidated that unilateral ANT DBS enhanced the seizure threshold by increasing the amount of REM sleep and decreasing the progressive enhancement of delta power during NREM sleep to suppress spontaneous seizure recurrences in PTZ kindling-induced epileptic rats. |
| first_indexed | 2024-12-21T11:55:48Z |
| format | Article |
| id | doaj.art-e14c0d7699714637a1093ed2b97f3fac |
| institution | Directory Open Access Journal |
| issn | 1664-2295 |
| language | English |
| last_indexed | 2024-12-21T11:55:48Z |
| publishDate | 2020-08-01 |
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| series | Frontiers in Neurology |
| spelling | doaj.art-e14c0d7699714637a1093ed2b97f3fac2022-12-21T19:04:56ZengFrontiers Media S.A.Frontiers in Neurology1664-22952020-08-011110.3389/fneur.2020.00752516603Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM SleepHsin-Tzu Tseng0Yi-Tse Hsiao1Pei-Lu Yi2Fang-Chia Chang3Fang-Chia Chang4Fang-Chia Chang5Fang-Chia Chang6Department of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University, Taipei, TaiwanDepartment of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University, Taipei, TaiwanDepartment of Sport Management, College of Tourism, Leisure and Sports, Aletheia University, Taipei, TaiwanDepartment of Veterinary Medicine, School of Veterinary Medicine, National Taiwan University, Taipei, TaiwanGraduate Institute of Brain and Mind Sciences, College of Medicine, National Taiwan University, Taipei, TaiwanGraduate Institute of Acupuncture Science, College of Chinese Medicine, China Medical University, Taichung City, TaiwanDepartment of Medicine, College of Medicine, China Medical University, Taichung City, TaiwanWe previously demonstrated that seizure occurrences at different zeitgeber times alter sleep and circadian rhythm differently. On the other hand, the synchronized delta wave of electroencephalogram (EEG) during non-rapid eye movement (NREM) sleep facilitates seizure, while the desynchronized EEG of rapid eye movement (REM) sleep suppresses it. We also elucidated that unilateral deep brain stimulation (DBS) of the anterior nucleus of thalamus (ANT) suppresses seizure recurrence. In the present study, we intraperitoneally injected pentylenetetrazol (PTZ, 40 mg/kg) for 14 consecutive days (PTZ kindling) to induce spontaneous seizure in rats, and a 30-min (delivered 10 min before each PTZ injection) or a 3-h DBS of unilateral ANT (delivered 1 h before each PTZ injection) was applied to suppress seizure. The frequency of DBS stimulation was 200 Hz and the electrical current consisted of biphasic square pulses with 50-μA intensity, 100-μs pulse width, and 4.1-ms stimulation interval. Our results found that PTZ-induced spontaneous seizure did not cause a significant change in the quantity of NREM sleep but suppressed the amount of REM sleep. Unilateral ANT DBS prolonged the onset latency of ictal seizure, decreased the spontaneous seizure duration, and increased the survival rate but did not change the amplitude of epileptiform EEGs during ictal period. Unilateral ANT DBS did not significantly alter NREM sleep but increased the amount of REM sleep. An analysis of the spectrograms of fast Fourier transform indicated that the intensities of all frequencies were enhanced during the PTZ-induced ictal period and the subsequent spontaneous seizure. Thirty minutes of unilateral ANT DBS suppressed the augmentation of low-frequency (<10 Hz) intensities during the spontaneous seizure induced by PTZ kindling. We further found that consecutive injections of PTZ progressively increased the enhancement of the delta powers during NREM sleep, whereas unilateral ANT DBS inhibited this progressive enhancement. It was also noticed that 30 min of ANT DBS exhibited a better efficacy in epilepsy suppression than 3 h of ANT DBS. These results elucidated that unilateral ANT DBS enhanced the seizure threshold by increasing the amount of REM sleep and decreasing the progressive enhancement of delta power during NREM sleep to suppress spontaneous seizure recurrences in PTZ kindling-induced epileptic rats.https://www.frontiersin.org/article/10.3389/fneur.2020.00752/fullanterior nucleus of thalamusdeep brain stimulationdelta powers during NREM sleepepilepsyREM sleepPTZ kindling |
| spellingShingle | Hsin-Tzu Tseng Yi-Tse Hsiao Pei-Lu Yi Fang-Chia Chang Fang-Chia Chang Fang-Chia Chang Fang-Chia Chang Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep Frontiers in Neurology anterior nucleus of thalamus deep brain stimulation delta powers during NREM sleep epilepsy REM sleep PTZ kindling |
| title | Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep |
| title_full | Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep |
| title_fullStr | Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep |
| title_full_unstemmed | Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep |
| title_short | Deep Brain Stimulation Increases Seizure Threshold by Altering REM Sleep and Delta Powers During NREM Sleep |
| title_sort | deep brain stimulation increases seizure threshold by altering rem sleep and delta powers during nrem sleep |
| topic | anterior nucleus of thalamus deep brain stimulation delta powers during NREM sleep epilepsy REM sleep PTZ kindling |
| url | https://www.frontiersin.org/article/10.3389/fneur.2020.00752/full |
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